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Received: 26 September 2018 | Revised: 1 March 2019 | Accepted: 7 March 2019 DOI: 10.1111/eva.12793 ORIGINAL ARTICLE A transcriptional and functional analysis of heat hardening in two invasive fruit fly species, Bactrocera dorsalis and Bactrocera correcta Xinyue Gu1 | Yan Zhao1 | Yun Su1 | Jiajiao Wu2 | Ziya Wang1 | Juntao Hu3,4 | Lijun Liu1 | Zihua Zhao1 | Ary A. Hoffmann5 | Bing Chen6 | Zhihong Li1 1Department of Entomology, College of Plant Protection, China Agricultural Abstract University, Beijing, China Many insects have the capacity to increase their resistance to high temperatures by 2 Guangdong Inspection and Quarantine undergoing heat hardening at nonlethal temperatures. Although this response is well Technology Center, Guangzhou, China 3Redpath Museum, McGill University, established, its molecular underpinnings have only been investigated in a few species Montreal, Quebec, Canada where it seems to relate at least partly to the expression of heat shock protein (Hsp) 4 Department of Biology, McGill University, genes. Here, we studied the mechanism of hardening and associated transcription Montreal, Quebec, Canada responses in larvae of two invasive fruit fly species in China, Bactrocera dorsalis and 5School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Bactrocera correcta. Both species showed hardening which increased resistance to Victoria, Australia 45°C, although the more widespread B. dorsalis hardened better at higher tempera‐ 6State Key Laboratory of Integrated Management of Pest Insects and Rodents, tures compared to B. correcta which hardened better at lower temperatures. Institute of Zoology, Chinese Academy of Transcriptional analyses highlighted expression changes in a number of genes repre‐ Sciences, Beijing, China senting different biochemical pathways, but these changes and pathways were in‐ Correspondence consistent between the two species. Overall B. dorsalis showed expression changes Zhihong Li, Department of Entomology, College of Plant Protection, China in more genes than B. correcta. Hsp genes tended to be upregulated at a hardening Agricultural University, Beijing, China. temperature of 38°C in both species, while at 35°C many Hsp genes tended to be Email: [email protected] and upregulated in B. correcta but not B. dorsalis. One candidate gene (the small heat Bing Chen, State Key Laboratory of shock protein gene, Hsp23) with a particularly high level of upregulation was investi‐ Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese gated functionally using RNA interference (RNAi). We found that RNAi may be more Academy of Sciences, Beijing, China. efficient in B. dorsalis, in which suppression of the expression of this gene removed Email: [email protected] and the hardening response, whereas in B. correcta RNAi did not decrease the hardening Ary A. Hoffmann, School of BioSciences, response. The different patterns of gene expression in these two species at the two Bio21 Institute, University of Melbourne, Parkville, Vic., Australia. hardening temperatures highlight the diverse mechanisms underlying hardening Email: [email protected] even in closely related species. These results may provide target genes for future Present address control efforts against such pest species. Bing Chen, College of Life Sciences, Hebei University, Baoding, China KEYWORDS expression plasticity, hardening response, Hsp23, invasive species, thermal adaptation Funding information National Natural Science Foundation of China, Grant/Award Number: 31772230 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd Evolutionary Applications. 2019;12:1147–1163. wileyonlinelibrary.com/journal/eva | 1147 1148 | GU ET AL. 1 | INTRODUCTION offspring performance as well as sharing a common origin. However, the geographical distribution of B. dorsalis is now much wider than During the invasive and adaptive process, species often encounter that of B. correcta both in China and elsewhere in the invasive range, novel environmental conditions that require adaptation through which B. dorsalis has invaded including Hawaii, Kenya, and Tahiti and genetically based evolutionary changes, phenotypic plasticity or a gradually displaced pre‐established Ceratitis species in recent years combination of these processes (Gibert et al., 2016; Vázquez, Gianoli, (Figure 1; Hu, Chen, & Li, 2014; Liu et al., 2014; Liu, Jin, & Ye, 2013; Morris, & Bozinovic, 2017). Phenotypic plasticity or evolutionary Lux, Copeland, White, Manrakhan, & Billah, 2003; Reitz & Trumble, changes can help buffer organisms from environmental changes and 2002). Thus far, there are no records of B. dorsalis being displaced by thereby help their establishment and expansion, and even be the tar‐ other tephritid fly species (Liu et al., 2017). get of selection (Wellband & Heath, 2017). Many studies that con‐ Temperature tolerance may be one of the key factors influencing sider the ability of plastic changes to buffer environmental effects the distribution of Tephritidae like B. dorsalis and B. correcta (Hu et consider temperature extremes, which play an important role in the al., 2014; Liu & Ye, 2009; Pieterse, Terblanche, & Addison, 2017; Qin, success of the invasive process (David et al., 1997; Delpuech et al., Ni, et al., 2015; Qin, Paini, Wang, Fang, & Li, 2015). B. dorsalis and 1995; Klepsatel et al., 2013). B. correcta have similar cold tolerance to C. capitata that is known to Resistance to extreme high temperature represents a complex be capable of adapting to a wide range of climates; however, B. cor‐ of traits that have been strongly affected by the environment ex‐ recta is more susceptible to heat than B. dorsalis (Hallman, Myers, perienced previously (Wos & Willi, 2018). Heat hardening is one El‐Wakkad, Tadrous, & Jessup, 2013; Hu et al., 2014; Myers, Cancio‐ component of resistance, involving the rapid induction of protec‐ Martinez, Hallman, Fontenot, & Vreysen, 2016; Papadopoulos, tive biochemical and physiological mechanisms, which markedly 2008). This may reflect species differences in thermal tolerance, enhance heat resistance (Malmendal et al., 2006). This process mediated through transcription changes involving genes such as of heat hardening in insects is regarded to be related to poten‐ Hsp70 and Hsp90 (Hu et al., 2014). For instance in Liriomyza, Hsp tial molecules, physiological changes or the differential expres‐ gene expression at different temperatures in two Liriomyza likely in‐ sion of genes, such as the expression of heat shock protein (Hsp) fluenced their geographical distribution (Huang & Kang, 2007; King genes (Borchel, Komisarczuk, Rebl, Goldammer, & Nilsen, 2018; & MacRae, 2015). Dahlgaard, Loeschcke, Michalak, & Justesen, 1998; Manjunatha, However, mechanisms that underpin heat hardening in Bactrocera Rajesh, & Aparna, 2010; Sisodia & Singh, 2006; Sørensen, species and how they might contribute to differences among the Kristensen, & Loeschcke, 2003; Willot, Gueydan, & Aron, 2017). species are poorly characterized. As in other insects, there are lim‐ The induction of genes such as Hsp varies with the intensity of ited data on how species might differ in gene transcription under thermal hardening stress and the insect's physiological state (King hardening and how any differences relate to temperature adaptation & MacRae, 2015). In Drosophila, hardening following a nonlethal and organism performance (Clarke, 2003). In this paper, we consid‐ heat stress activates a heat shock response through altering the ered whether differences in temperature adaptability associated transcription and translation of a set of genes including small with hardening are linked to the regulation of certain genes or path‐ Hsp genes (sHsps) and other Hsps including Hsp70 (DiDomenico, ways, which in turn has contributed to the different distribution and Bugaisky, & Lindquist, 1982; Malmendal et al., 2006; Sørensen, Nielsen, Kruhøffer, Justesen, & Loeschcke, 2005). Other insects whose hardening responses have been characterized include the armyworm Mythimna separata, where preheating larvae enhances expression of genes encoding superoxide dismutase 1, catalase and Hsp70, the whitefly Bemisia tabaci, where Hsp23, 70 and 90 are upregulated, and the ant Cataglyphis mauritanica, where hard‐ ening is associated with the expression of two Hsc70‐4 cognates (Díaz, Orobio, Chavarriaga, & Toro‐Perea, 2015; Matsumura, Matsumoto, & Hayakawa, 2017; Willot et al., 2017). Bactrocera dorsalis (Hendel) and B. correcta (Bezzi) (Diptera: Tephritidae) are invasive pests that damage fruits and vegetables (Permpoon, Aketarawong, & Thanaphum, 2011). These species have been investigated because of their increasingly wide distributions and repeated invasions. The Bactrocera genus has a competitive advantage for oviposition over other fruit flies such as Ceratitis FIGURE 1 Global distribution map of Bactrocera correcta and B. dorsalis. The global distribution of the two species based on the capitata which is one of the most devastating and invasive world‐ information from GBIF (https://www.gbif.org/) and CABI (https:// wide pests (Liu, Zhang, Hou, Ou‐Yang, & Ma, 2017; Malacrida et www.cabi.org/). The blue dots and areas represent the distribution al., 2007). The two Bactrocera species are similar in many biologi‐ of B. correcta,
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